Immunomodulatory parasites and toll-like receptor-mediated tumour necrosis factor alpha responsiveness in wild mammals

Jackson, Joe; Friberg, Ida M.; Bolch, Luke; Lowe, Ann; Ralli, Catriona; Harris, P. D.; Behnke, Jerzy M.; Bradley, Janette E.

doi:10.1186/1741-7007-7-16

Cited by 68 publications

(116 citation statements)

References 74 publications

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“…We used the restricted data set for the northern 'massif des Ardennes' where we previously found a significant association between PUUV and H. mixtum (Ribas . Several studies on laboratory mice and wild rodents have shown that a phylogenetically closely related helminth species, Heligmosomoides polygyrus, may be immunosuppressive (Jackson et al, 2009;Maizels et al, 2012). This suggested that infection with H. mixtum might modulate the immune responses of bank voles and change their susceptibility to PUUV.…”

Section: Methodsmentioning

confidence: 99%

“…In particular, Heligmosomoıdes polygyrus bakeri has been shown to induce a wide spectrum of immunomodulatory effects in the laboratory mouse and to affect the outcome of infection with several pathogens, including nematodes, trematodes, protozoa and bacteria (see a recent review by Maizels et al, 2012). Jackson et al (2009) even showed, in wild wood mice (Apodemus sylvaticus), that the Tnf-a response to TLR ligands was downregulated by natural infection with H. polygyrus. It has been suggested that H. mixtum may also be immunosuppressive.…”

Section: Epidemiological Consequences For Puuv Infectionmentioning

confidence: 99%

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Landscape features and helminth co-infection shape bank vole immunoheterogeneity, with consequences for Puumala virus epidemiology

et al. 2013

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Heterogeneity in environmental conditions helps to maintain genetic and phenotypic diversity in ecosystems. As such, it may explain why the capacity of animals to mount immune responses is highly variable. The quality of habitat patches, in terms of resources, parasitism, predation and habitat fragmentation may, for example, trigger trade-offs ultimately affecting the investment of individuals in various immunological pathways. We described spatial immunoheterogeneity in bank vole populations with respect to landscape features and co-infection. We focused on the consequences of this heterogeneity for the risk of Puumala hantavirus (PUUV) infection. We assessed the expression of the Tnf-a and Mx2 genes and demonstrated a negative correlation between PUUV load and the expression of these immune genes in bank voles. Habitat heterogeneity was partly associated with differences in the expression of these genes. Levels of Mx2 were lower in large forests than in fragmented forests, possibly due to differences in parasite communities. We previously highlighted the positive association between infection with Heligmosomum mixtum and infection with PUUV. We found that Tnf-a was more strongly expressed in voles infected with PUUV than in uninfected voles or in voles co-infected with the nematode H. mixtum and PUUV. H. mixtum may limit the capacity of the vole to develop proinflammatory responses. This effect may increase the risk of PUUV infection and replication in host cells. Overall, our results suggest that close interactions between landscape features, co-infection and immune gene expression may shape PUUV epidemiology.

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Section: Methodsmentioning

confidence: 99%

Section: Epidemiological Consequences For Puuv Infectionmentioning

confidence: 99%

Landscape features and helminth co-infection shape bank vole immunoheterogeneity, with consequences for Puumala virus epidemiology

et al. 2013

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“…However, maternal effects and other early-life experiences, including pathogen exposure, could contribute to these differences (Saino et al, 2002;Jackson et al, 2009;Morrison et al, 2009). For instance, maternal transfer of hormones or other molecules to eggs can influence physiological, behavioral and immunological phenotypes in offspring (Saino et al, 2002;Groothuis et al, 2005;Grindstaff et al, 2006;Gasparini et al, 2009;Hasselquist and Nilsson, 2009).…”

Section: Evolved Versus Plastic Differences In the Acute Phase Responsementioning

confidence: 99%

“…Revealing these mechanisms will help us understand how and where selection acts to shape diversity in immunological and life history investments (Zera and Harshman, 2001). Moreover, uncovering the mechanisms responsible for this diversity may help identify predictive biomarkers of host resistance (Poland et al, 2008;Vollmer-Conna et al, 2008), clarify the impact of different parasitic organisms on host defenses (Jackson et al, 2009), and provide important tools for forecasting and mitigating the spread of wildlife diseases.…”

Section: Introductionmentioning

confidence: 99%

Population differences in fever and sickness behaviors in a wild passerine: a role for cytokines

Adelman

Bentley

Wingfield

et al. 2010

Journal of Experimental Biology

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SUMMARYImmune responses benefit hosts by clearing pathogens, but they also incur physiological costs and tissue damage. While wild animals differ in how they balance these costs and benefits, the physiological mechanisms underlying such differential investment in immunity remain unknown. Uncovering these mechanisms is crucial to determining how and where selection acts to shape immunological defense. Among free-living song sparrows (Melospiza melodia) in western North America, sicknessinduced lethargy and fever are more pronounced in Southern California than in Washington and Alaska. We brought song sparrows from two populations (Southern California and Washington) into captivity to determine whether these differences persist in a common environment and what physiological signals facilitate such differences. As in free-living sparrows, captive California birds exhibited more pronounced fever and lethargy than Washington birds in response to lipopolysaccharide, a nonpathogenic antigen that mimics bacterial infection. After treatment, the two populations showed similar reductions in luteinizing hormone levels, food intake and body mass, although treated birds from California lost more breast muscle tissue than treated birds from Washington. Moreover, California birds displayed higher bioactivity of interleukin-6, a pro-inflammatory cytokine, and marginally higher levels of corticosterone, a steroid hormone involved in stress, metabolism and regulating inflammatory responses. Our results show that immunological differences between these populations cannot be explained by immediate environment alone and may reflect genetic, maternal or early-life effects. Additionally, they suggest that cytokines play a role in shaping immunological variation among wild vertebrates. Supplementary material available online at

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“…Mite-induced immuno-modulation of the host is a possibility (Jackson et al, 2009) and recent research suggests that D. gallinae both adapts its reproductive behaviour to the host (Harrington et al, 2010a) and modulates the host initial inflammatory responses (Harrington et al, 2010a,b). An understanding of the immunology of the D. gallinae-host relationship is important where vaccination is proposed as a control measure, yet despite the importance of D. gallinae in poultry production there is a lack of understanding of how the mite modulates and/or stimulates host immunity.…”

Section: Vaccinesmentioning

confidence: 99%

Opportunities for integrated pest management to control the poultry red mite, Dermanyssus gallinae

Harrington

George

Guy

et al. 2011

World's Poultry Science Journal

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Dermanyssus gallinae is the most economically important ectoparasite of laying hens in Europe. Control of D. gallinae is already hampered by issues of pesticide resistance and product withdrawal. With the prohibition of conventional cages in 2012 and the resulting switch to more structurally complex housing which favours red mite, the importance of managing this pest is expected to increase. Integrated Pest Management (IPM), as often employed in agricultural pest control, may be a way to address these issues where a combination of different novel control methods could be used with/without conventional management techniques to provide a synergistic and more efficacious effect. Work at in our laboratory has shown that essential oils, including thyme and garlic, may act as effective D. gallinae repellents and acaricides, whilst preliminary vaccine studies have demonstrated a significant increase in mite mortality in vitro using concealed antigens. Work elsewhere has considered predators and fungi for D. gallinae control and other husbandry techniques such as manipulating temperature and lighting regimes in poultry units. This paper will review the available and emerging techniques for D. gallinae control and discuss which techniques might be suitable for inclusion in an integrated management programme (e.g. synthetic acaricides and diatomaceous earths).

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Immunomodulatory parasites and toll-like receptor-mediated tumour necrosis factor alpha responsiveness in wild mammals

Cited by 68 publications

References 74 publications

Landscape features and helminth co-infection shape bank vole immunoheterogeneity, with consequences for Puumala virus epidemiology

Landscape features and helminth co-infection shape bank vole immunoheterogeneity, with consequences for Puumala virus epidemiology

Population differences in fever and sickness behaviors in a wild passerine: a role for cytokines

Opportunities for integrated pest management to control the poultry red mite, Dermanyssus gallinae

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